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A neural correlate of response bias in monkey caudate nucleus

Nature volume 418, pages 413–417 (2002)Cite this article

Abstract

Primates are equipped with neural circuits in the prefrontal cortex1,2,3,4,5,6, the parietal cortex7 and the basal ganglia6,8,9,10,11 that predict the availability of reward during the performance of behavioural tasks. It is not known, however, how reward value is incorporated in the control of action. Here we identify neurons in the monkey caudate nucleus that create a spatially selective response bias depending on the expected gain. In behavioural tasks, the monkey had to make a visually guided eye movement in every trial, but was rewarded for a correct response in only half of the trials. Reward availability was predictable on the basis of the spatial position of the visual target. We found that caudate neurons change their discharge rate systematically, even before the appearance of the visual target, and usually fire more when the contralateral position is associated with reward. Strong anticipatory activity of neurons with a contralateral preference is associated with decreased latency for eye movements in the contralateral direction. We conclude that this neuronal mechanism creates an advance bias that favours a spatial response when it is associated with a high reward value.

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Figure 1: Experimental design of the biased saccade task (BST).
Figure 2: Effect of position-reward mapping on caudate anticipatory activity.
Figure 3: Adaptation of behaviour and neuronal activity to a reversal of the position-reward contingency.
Figure 4: Comparison between the cued saccade task (CST) and the biased saccade task (BST).

References

  1. Amador, N., Schlag-Rey, M. & Schlag, J. Reward-predicting and reward-detecting neuronal activity in the supplementary eye field. J. Neurophysiol. 84, 2166–2170 (2000)

    Article  CAS  Google Scholar 

  2. Kobayashi, S., Lauwereyns, J., Koizumi, M., Sakagami, M. & Hikosaka, O. Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex. J. Neurophysiol. 87, 1488–1498 (2002)

    Article  Google Scholar 

  3. Leon, M. I. & Shadlen, M. N. Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque. Neuron 24, 415–425 (1999)

    Article  CAS  Google Scholar 

  4. Tremblay, L. & Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704–708 (1999)

    Article  ADS  CAS  Google Scholar 

  5. Watanabe, M. Reward expectancy in primate prefrontal neurons. Nature 382, 629–632 (1996)

    Article  ADS  CAS  Google Scholar 

  6. Rolls, E. T. The Brain and Emotion (Oxford Univ. Press, New York, 1999)

    Google Scholar 

  7. Platt, M. L. & Glimcher, P. W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999)

    Article  ADS  CAS  Google Scholar 

  8. Hikosaka, O., Sakamato, M. & Usui, S. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J. Neurophysiol. 61, 814–832 (1989)

    Article  CAS  Google Scholar 

  9. Kawagoe, R., Takikawa, Y. & Hikosaka, O. Expectation of reward modulates cognitive signals in the basal ganglia. Nature Neurosci. 1, 411–416 (1998)

    Article  CAS  Google Scholar 

  10. Schultz, W., Apicella, P., Scarnati, E. & Ljungberg, T. Neuronal activity in monkey ventral striatum related to the expectation of reward. J. Neurosci. 12, 4595–4610 (1992)

    Article  CAS  Google Scholar 

  11. Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997)

    Article  CAS  Google Scholar 

  12. Bindra, D. Neuropsychological interpretation of the effects of drive and incentive-motivation on general activity and instrumental behaviour. Psychol. Rev. 75, 1–22 (1968)

    Article  Google Scholar 

  13. Dickinson, A. & Baleine, B. Motivational control of goal-directed action. Anim. Learn. Behav. 22, 1–18 (1994)

    Article  Google Scholar 

  14. Watanabe, M. et al. Behavioral reactions reflecting differential reward expectations in monkeys. Exp. Brain Res. 140, 511–518 (2001)

    Article  CAS  Google Scholar 

  15. Apicella, P., Scarnati, E., Ljungberg, T. & Schultz, W. Neuronal activity in monkey striatum related to the expectation of predictable environmental events. J. Neurophysiol. 68, 945–960 (1992)

    Article  CAS  Google Scholar 

  16. Rolls, E. T., Thorpe, S. J. & Maddison, S. P. Responses of striatal neurons in the behaving monkey. I. Head of the caudate nucleus. Behav. Brain Res. 7, 179–210 (1983)

    Article  CAS  Google Scholar 

  17. Hikosaka, O., Sakamato, M. & Usui, S. Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. J. Neurophysiol. 61, 780–798 (1989)

    Article  CAS  Google Scholar 

  18. Kawaguchi, Y., Wilson, C. J. & Emson, P. C. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J. Neurosci. 10, 3421–3438 (1990)

    Article  CAS  Google Scholar 

  19. Fisher, R. S., Buchwald, N. A., Hull, C. D. & Levine, M. S. The GABAergic striatonigral neurons of the cat: Demonstration by double peroxidase labeling. Brain Res. 398, 148–156 (1986)

    Article  CAS  Google Scholar 

  20. Hikosaka, O. & Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. J. Neurophysiol. 49, 1268–1284 (1983)

    Article  CAS  Google Scholar 

  21. Lauwereyns, J. et al. Feature-based anticipation of cues that predict reward in monkey caudate nucleus. Neuron 33, 463–473 (2002)

    Article  CAS  Google Scholar 

  22. Takikawa, Y., Kawagoe, R. & Hikosaka, O. Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. J. Neurophysiol. 87, 508–515 (2002)

    Article  Google Scholar 

  23. Rescorla, R. A. & Wagner, A. R. in Classical Conditioning II: Current Research and Theory (eds Black, A. H. & Prokasy, W. F.) 64–99 (Appleton Century Crofts, New York, 1972)

    Google Scholar 

  24. Basso, M. A. & Wurtz, R. H. Modulation of neuronal activity by target uncertainty. Nature 389, 66–69 (1997)

    Article  ADS  CAS  Google Scholar 

  25. Dorris, M. C. & Munoz, D. P. Saccadic probability influences motor preparation signals and time to saccadic initiation. J. Neurosci. 18, 7015–7026 (1998)

    Article  CAS  Google Scholar 

  26. Hikosaka, O., Kawagoe, R. & Takikawa, Y. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80, 953–978 (2000)

    Article  CAS  Google Scholar 

  27. Ikeda, T., Takikawa, Y. & Hikosaka, O. Visuo-motor and anticipatory activities of monkey superior colliculus neurons are modulated by reward. Soc. Neurosci. Abstr. 27, 59.1 (2001)

    Google Scholar 

  28. Sato, M. & Hikosaka, O. Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement. J. Neurosci. 22, 2363–2373 (2002)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank H. Nakahara, Y. Shimo, M. Sato, Y. Takikawa, R. Kawagoe, H. Itoh, S. Kobayashi, M. Koizumi and M. Sakagami for comments and technical assistance. This research was supported by the Japanese Society for the Promotion of Science.

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Authors and Affiliations

  1. Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, USA, Building 49, Room 2A50, Bethesda, Maryland, 20892

    Johan Lauwereyns, Katsumi Watanabe & Okihide Hikosaka

  2. Department of Physiology, Juntendo University, Bunkyo-ku, Tokyo, 2-1-1 Hongo, 113-0033, Japan

    Brian Coe

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  1. Johan Lauwereyns
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  2. Katsumi Watanabe
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  4. Okihide Hikosaka
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Correspondence to Okihide Hikosaka.

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Lauwereyns, J., Watanabe, K., Coe, B. et al. A neural correlate of response bias in monkey caudate nucleus. Nature 418, 413–417 (2002). https://doi.org/10.1038/nature00892

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